Download Is maize B chromosome preferential fertilization controlled by a

Heredity 86 (2001) 743±748
Received 10 July 2000, accepted 29 March 2001
Is maize B chromosome preferential
fertilization controlled by a single gene?
 NICA GONZAÂLEZ-SA
 NCHEZ , LIDIA POGGIOà§,
A. MAURICIO CHIAVARINOà, MO
MARIÂA J. PUERTAS* , MARCELA ROSATOà & PABLO ROSIà§
Departamento de GeneÂtica, Facultad de BiologõÂa, Universidad Complutense, 28040 Madrid, Spain,
àInstituto FitoteÂcnico de Santa Catalina (FCAF, UNLP)-Centro de Investigaciones GeneÂticas
(UNLP-CONICET-CIC), C.C. 41836 Llavallol, Buenos Aires, Argentina and §Departamento de BiologõÂa,
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina
In previous work, genotypes for high and low B chromosome transmission rate were selected from a
native race of maize. It was demonstrated that the B transmission is genetically controlled. The
present work reports the fourth and ®fth generations of selection and the F1 hybrids between the lines.
The native B is characterized by a constant behaviour, with normal meiosis and nondisjunction in
100% of postmeiotic mitosis. It is concluded that genetic variation for B transmission between the
selected lines is due to the preferential fertilization process. The F1 hybrids show intermediate B
transmission rate between the lines. They are uniform, the variance of the selected character being one
order of magnitude lower than that of the native population. In addition, 0B ´ 2B and 2B ´ 2B
crosses were made to study the e€ect of the presence of B chromosomes in the female parent, resulting
in non-signi®cant di€erences. Several crosses were made both in Buenos Aires and in Madrid to
compare the possible environmental e€ect, but signi®cant di€erences were not found. Our results are
consistent with the hypothesis of a single major gene controlling B transmission rate in maize, which
acts in the egg cell at the haploid level during fertilization. It is also hypothesized that maize Bs use the
normal maize fertilization process to promote their own transmission.
Keywords: B-chromosomes, maize, preferential fertilization, Zea mays.
somes of the normal set (A chromosomes, As). The A
fragment of the BA chromosome carries genetic markers
which reveal the presence of the B. In this way, tedious
cytological screening for the Bs is unnecessary. Consequently, maize native Bs are poorly known at the
population level.
In 1993 a selection process was initiated to study the
cytological features and the genetic control of maize B
transmission in the native race Pisingallo from Argentina, where the Bs are present in 44% of the individuals.
It was demonstrated that B transmission rate (B-TR) is
genetically controlled, both on the female and male
sides, and genotypes were isolated that control high (H)
and low (L) B-TR (Rosato et al., 1996). It was later
demonstrated that the genes controlling male B-TR are
located on the A chromosomes, because in female
0B ´ male 2B crosses, the B-TR depends on the H or L
status of the 0B female parent (Chiavarino et al., 1998).
The results of that work also showed that preferential
fertilization by the 2B-carrying sperm nucleus does not
always occur, so that in 0B female parents of the H
genotype the frequency of fertilization by the 2B sperm
Introduction
The numerical polymorphism for the B chromosomes
(Bs) of maize is maintained by three main processes:
(i) B nondisjunction at the second pollen grain mitosis,
which produces sperm nuclei with di€erent B numbers
(Roman, 1947; Carlson, 1978; Carlson & Chou, 1981);
(ii) preferential fertilization by the sperm nucleus carrying the Bs after the nondisjunction process (Roman,
1948; Carlson, 1969); and (iii) the suppression of meiotic
loss when the Bs are unpaired (Carlson & Roseman,
1992).
Beckett (1982) proposed a higher competitive ability
of B-carrying pollen grains as an additional mechanism
to maintain the Bs in maize. However, Carlson (1997)
reported results that do not show a clear advantage of
B-carrying pollen over normal pollen.
Most of these features and other properties of maize
Bs have been studied taking advantage of lines carrying
reciprocal translocations between the Bs and chromo*Correspondence. E-mail: [email protected]
Ó 2001 The Genetics Society of Great Britain.
743
744
A. M. CHIAVARINO ET AL.
3 0B and 2B plants obtained from 0B H ´ 2B L crosses,
that we call HL hybrids, were used to make both
0B HL ´ 2B HL and 2B HL ´ 2B HL crosses.
4 0B and 2B plants obtained from 0B L ´ 2B H crosses,
that we call LH hybrids, were used to make both
0B LH ´ 2B LH and 2B LH ´ 2B LH crosses.
The crosses described in 1 and 2 were made both in
Buenos Aires (Argentina) and Madrid (Spain). Crosses
described in 3 and 4 were made in Madrid. In Buenos
Aires the plants were grown in the greenhouse of the
IFSC (Universidad Nacional de La Plata) whereas in
Madrid the plants grew outside, in the experimental ®eld
of the Complutense University.
To score for B chromosome number, the primary
root tips were pretreated with 0.002 mol/L 8-hydroxyquinoline for 3 h at 20±22°C, subsequently ®xed in
ethanol : acetic acid 3 : 1 and stained by the Feulgen
method.
is increased, but in the L genotype fertilization by the 0B
or 2B sperm nucleus is at random, resulting in a
Mendelian B-TR.
The present work reports the results of the fourth and
®fth generations of selection (G4 and G5) for H and L
male B-TR. We report the behaviour of the HL and LH
F1 hybrids. In addition, 0B ´ 2B and 2B ´ 2B crosses
were made to study the e€ect of the presence of B
chromosomes in the female parent on male B-TR.
Several of these crosses were made both in Spain and
Argentina to study possible environmental e€ects.
Materials and methods
The materials used were selected lines of maize, Zea mays
ssp. mays. The lines were obtained from crosses female
0B ´ male 2B, whose progeny was selected for high and
low B transmission rate during ®ve generations. These
lines were actually selected for H or L male B-TR because
the Bs were always transmitted on the male side. The
selection process was carried out following the method
described in Rosato et al. (1996) and in Chiavarino et al.
(1998). The original material, from which the selection
was initiated, belongs to the native race Pisingallo from
NW Argentina (Rosato et al., 1998).
In all crosses mentioned in the following, the female
parent will be indicated ®rst; for example, a 0B ´ 2B
cross means that the female parent had 0B and the male
parent had 2B. Similarly, an HL hybrid is that obtained
using a plant of the H line as female and a plant of the L
line as male.
We used the following genotypes and crosses:
1 0B and 2B plants of the third and fourth generation of
selection for high B-TR in 0B H ´ 2B H crosses, were
used to make both 0B H ´ 2B H (which correspond to
the fourth and ®fth generation of selection, respectively)
and 2B H ´ 2B H crosses.
2 The same as in 1 but using the L line.
Results
Table 1 shows the results of the crosses made in Madrid.
The progeny obtained in crosses 0B ´ 2B allows deduction of the transmission of B chromosomes on the male
side. Nearly all the progeny carried either 0 or 2 Bs
indicating that nondisjunction occurred in 100% of the
cases, because 1B plants were not found. Only one out
of 640 plants (0.16%) had 4 Bs, in all probability, by
lack of proper segregation at meiosis followed by
nondisjunction of both Bs. This low frequency of B
transmission irregularities shows that in this native race
the Bs have a remarkably constant behaviour at male
meiosis and pollen mitosis, characterized by the segregation of the two Bs to opposite poles in more than 99%
of the anaphase I cells and nondisjunction of the single
B in 100% of postmeiotic mitoses.
Male B-TR in 0B ´ 2B crosses was estimated by
dividing the number of B-carrying plants in the progeny
Table 1 B transmission in 0B ´ 2B and 2B ´ 2B maize crosses made in Madrid
0
H´H
HL ´ HL
LH ´ LH
L´L
6
6
6
7
39
64
71
94
H´H
HL ´ HL
LH ´ LH
L´L
9
9
8
7
1
9
8
6
Type of cross
0B ´ 2B
2B ´ 2B
No. of Bs in the progeny
No. of
crosses
1
2
3
109
94
86
82
39
78
69
85
11
15
13
7
4
5
1
174
119
111
69
6
9
5
5
1
1
1
Total
Mean male
B-TR ‹ SE
148
158
157
177
0.734
0.578
0.548
0.469
‹
‹
‹
‹
0.037
0.020
0.013
0.033
232
231
207
172
0.819
0.593
0.537
0.449
‹
‹
‹
‹
0.018
0.015
0.067
0.032
Unexpected
progeny
(mean ‹ SE)
0.076
0.144
0.123
0.101
‹
‹
‹
‹
0.019
0.019
0.035
0.026
B-TR, B transmission rate.
Ó The Genetics Society of Great Britain, Heredity, 86, 743±748.
MAIZE B CHROMOSOME TRANSMISSION
by the total number of plants scored. It should be noted
that the selected character `B transmission rate' is not
measured in the individuals themselves, but in their
progenies. Therefore, B-TR in both HL and LH F1
hybrids is estimated in HL ´ HL and LH ´ LH crosses,
respectively.
The mean B-TR varies between the di€erent types of
cross, H ´ H being the highest value and L ´ L the
lowest. It is important to determine if the HL and LH F1
hybrids show dominance or if they behave as intermediates. To test whether the observed distribution of B
chromosomes in the progenies of HL ´ HL and
LH ´ LH is intermediate between H ´ H and L ´ L
(null hypothesis), the weighted distribution between
H ´ H and L ´ L was calculated (68.95 of 0B and 94.84
of 2B) and compared to that observed in HL ´ HL and
in LH ´ LH with a v2 contingency test. In both cases the
di€erences were nonsigni®cant (P ˆ 0.98 and P ˆ 0.57,
respectively), whereas the weighted distribution was
signi®cantly di€erent from both H ´ H and L ´ L
distributions (P ˆ 0.003 and P ˆ 0.04, respectively).
It is interesting to note that the variance of the character
was low in the F1 hybrids and in the lines crossed to obtain
them (V ˆ 0.002, V ˆ 0.007, V ˆ 0.007 and V ˆ 0.009 in
HL, LH, H and L, respectively). In contrast, the variance
of the character in the native population was one order of
magnitude higher (V ˆ 0.063). This indicates that the F1 is
remarkably uniform, as expected for an F1 between two
homozygous lines.
Table 1 also shows the results of 2B ´ 2B crosses
made in Madrid. If the two Bs had a regular meiotic
segregation during megasporogenesis, 2B plants should
always transmit 1B, because it has been reported that B
nondisjunction does not occur on the female side
(Randolph, 1941; reviewed in Jones & Rees, 1982).
Therefore, as 2B plants transmit 0B and 2B male
gametes in nearly all cases (upper part of Table 1), the
expected progeny in 2B ´ 2B crosses consists of plants
carrying only odd B numbers: 1B and 3B at high
frequency, and less than 1% 5B plants. However,
unexpected 0, 2 and 4B plants were obtained, which
demonstrates that irregularities occur at female gametogenesis, producing 0B and 2B female gametes.
The frequency of unexpected progeny is shown in the
last column of Table 1. One-way ANOVA showed that
di€erences between the four types of crosses were
nonsigni®cant (F3,29 ˆ 1.45, P ˆ 0.25).
In 2B ´ 2B crosses, we cannot estimate male B
transmission rate accurately with the available data,
because it is not possible to determine if the two Bs of
the 2B progeny come from the male or the female
gametes. To avoid this problem partially, we calculated
the minimum estimate of male B-TR, dividing the
number of plants carrying 3 or more Bs by the total
Ó The Genetics Society of Great Britain, Heredity, 86, 743±748.
745
number of plants of the progeny, assuming that all 2B
plants received the Bs from the female gamete.
It is evident that the mean B-TR varied between the
four types of 2B ´ 2B crosses, H ´ H having the highest
value and L ´ L the lowest. To test whether the
observed B distribution in the progenies of HL ´ HL
and LH ´ LH was intermediate between H ´ H and
L ´ L, the weighted distribution between H ´ H and
L ´ L was calculated (3.13 of 0B, 58.6 of 1B, 9.29 of 2B,
129.3 of 3B and 6.15 of 4 + 5B) and compared to that
observed in HL ´ HL and LH ´ LH using a v2 contingency test. In both cases the di€erences were nonsigni®cant (P ˆ 0.15 and P ˆ 0.25, respectively), whereas the
weighted distribution was signi®cantly di€erent from
both H ´ H and L ´ L distributions (P ˆ 0.03 and
P < 0.001, respectively).
A two-way ANOVA was made comparing the mean
B-TRs shown in Table 1 (dependent variable) with the
genotype of the crosses (H ´ H, HL ´ HL, LH ´ LH or
L ´ L) and the presence/absence of Bs in the female
parent (0B ´ 2B or 2B ´ 2B crosses) as factors. Only the
genotype of the cross had a highly signi®cant e€ect
(F3,50 ˆ 51.06, P < 0.0001), whereas the presence of Bs
in the female parent and the interaction were nonsigni®cant (F1,50 ˆ 3.14, P ˆ 0.082; F3,50 ˆ 1.54, P ˆ 0.214,
respectively).
In addition, we performed a Sche€e post-hoc test,
which showed that the mean B-TR in HL ´ HL did not
di€er from that of LH ´ LH, whereas both were
signi®cantly di€erent from that of H ´ H and L ´ L.
This is a second way to see that HL and LH hybrids
behave as intermediate types.
Table 2 shows the results obtained in the 0B ´ 2B and
2B ´ 2B crosses made in Buenos Aires. A two-way ANOVA
was made with B-TR as dependent variable and the
genotype of the crosses (H ´ H or L ´ L) and the
presence/absence of Bs in the female parent (0B ´ 2B or
2B ´ 2B crosses) as factors. As in the previous case only
the genotype had a highly signi®cant e€ect (F1,27 ˆ 41.9,
P < 0.0001), whereas both the presence/absence of
Bs in the female parent and the interaction were nonsigni®cant (F1,27 ˆ 0.051, P ˆ 0.823; F1,27 ˆ 0.018, P ˆ 0.893,
respectively).
The crosses made in Buenos Aires and Madrid were
compared by a three-way ANOVA. The dependent
variable was B-TR, and the factors were the genotype
of the crosses (H ´ H or L ´ L; F1,53 ˆ 112.76,
P < 0.0001); the presence of Bs in the female parent
(0B ´ 2B or 2B ´ 2B; F1,53 ˆ 0.21, P ˆ 0.648); and
the locality (Buenos Aires or Madrid; F1,53 ˆ 1.42,
P ˆ 0.239). The interactions were nonsigni®cant in all
cases (interaction genotype ´ female parent, F1,53 ˆ 0.63,
P ˆ 0.430; interaction genotype ´ locality, F1,53 ˆ 3.10,
P ˆ 0.084; interaction female parent ´ locality, F1,53 ˆ
746
A. M. CHIAVARINO ET AL.
Table 2 B transmission in 0B ´ 2B and 2B ´ 2B maize crosses made in Buenos Aires
Type of cross
No. of Bs in the progeny
No. of
crosses
0
0B ´ 2B
H´H
L´L
8
8
56
107
2B ´ 2B
H´H
L´L
7
8
2
6
1
2
3
4
141
97
47
96
5
3
121
86
7
7
Unexpected
progeny
(mean ‹ SE)
Total
Mean male
B-TR ‹ SE
197
204
0.711 ‹ 0.038
0.472 ‹ 0.044
182
198
0.725 ‹ 0.028 0.074 ‹ 0.016
0.475 ‹ 0.036 0.082 ‹ 0.019
B-TR, B transmission rate.
polymorphism for B chromosomes is genetically controlled in maize. As it was stated in the introduction, there
are three main factors in¯uencing the polymorphism: (i) B
nondisjunction at the second pollen mitosis; (ii) preferential fertilization by the sperm nucleus carrying the Bs; and
(iii) prevention of the meiotic B loss. Our selection
experiments provide insights into the three items.
(i) B nondisjunction
Fig. 1 Results of the selection process for high (H) and low (L)
male B transmission rate (B-TR) along ®ve generations (G1±5)
in the native race Pisingallo (G0) of maize.
0.67, P ˆ 0.418; interaction genotype ´ female parent ´
locality, F1,53 ˆ 1.63, P ˆ 0.207).
The result of the whole selection process is shown in
Fig. 1. Data of the native Pisingallo population (G0) and
G1 were reported by Rosato et al. (1996). G2 and G3
were reported by Chiavarino et al. (1998) and G4 and G5
are reported in the present paper. B-TR values were
signi®cantly di€erent between the H and L lines in every
generation. Regression of G1 to G5 was calculated, and
the slope was signi®cant in the H line (b ˆ 0.020 ‹ 0.01,
P ˆ 0.031) and nonsigni®cant in the L line (b ˆ 0.013 ‹
0.009, P ˆ 0.078). It seems therefore that more selection
gain in the H line might be expected in further generations, whereas this is not so in the L line.
Discussion
The process of selection for H or L B-TR in maize
was designed to answer the question of how the
Carlson (1997) pointed out that B±A translocations have
been extensively used in experiments to study maize B
chromosomes and, consequently, the B has been almost
always studied in the translocated form. However,
important features of the B chromosome are di€erent
in the native and translocated forms. For example,
variation in B nondisjunction frequency was described
by Rusche et al. (1997) using a molecular probe to detect
the presence, location and frequency of B chromosomes
in interphase nuclei of pollen grains. These authors
found, in the TB-10 L18 B±A translocation, that nondisjunction of the B centromere occurred at an average
frequency of 56.6%. This is consistent with genetic
studies using the same B±A translocation, where deletions created by the translocation breakpoints were used
to establish the region involved in the nondisjunction
process (Lin, 1978, 1979). In contrast, our results,
obtained by scoring for B number in hundreds of plants,
show that the native B undergoes nondisjunction in
100% of the cases because in 0B ´ 2B crosses not a single
1B plant was found. From our present results it can be
concluded that the behaviour of the native B during
gametogenesis is consistently repeatable, almost always
producing 0B and 2B sperm nuclei.
As there is no variation for the character `B nondisjunction at second pollen mitosis' in the native race
studied, it is not possible to determine its genetic control
by selection methods. In all probability, the chromosome regions controlling B nondisjunction described by
Carlson (1978) and Carlson & Chou (1981) are ®xed in
the native race Pisingallo.
Ó The Genetics Society of Great Britain, Heredity, 86, 743±748.
MAIZE B CHROMOSOME TRANSMISSION
(ii) and (iii) Preferential fertilization
and prevention of meiotic B loss
The variation observed in the selected character
`B transmission rate', is undoubtedly due to variation
in preferential fertilization. This conclusion is based on
two observations. (i) Chiavarino et al. (1997) reported
that in 2B plants the Bs formed bivalents in about 90%
of the metaphase I cells, irrespective of their H or L
status and the generation of selection studied. On the
other hand, the number of micronuclei at the tetrad
stage was lower than 5% in all cases. It was concluded
that the di€erential B transmission on the male side was
not due to a di€erential B gain or loss at male meiosis.
(ii) Since a 100% B nondisjunction produces only 0B
and 2B sperm nuclei in a 1 : 1 ratio, the high or low
B-TR needs to be achieved in a later stage, most likely
by di€erential fertilization success of both sperm nucleus
types.
Considering the results of the selection process
carried out for the character high or low B-TR during
®ve consecutive generations (Fig. 1), it can be observed
®rstly, that the L line is characterized by a Mendelian
B-TR (0.5), whereas the H line shows a higher than
Mendelian B-TR (about 0.7). Secondly, that all detectable selection gain in the L line, and most of that of
the H line, was obtained in the ®rst generation of
selection. The simplest explanation for this result is
that a single major gene with two alleles (H and L) is
controlling the selected character. Thus, most plants
obtained in the ®rst generation were the two HH and
LL homozygotes. This conclusion is also consistent
with the low variance of the selected character in both
F1 HL and LH hybrids, as expected in a uniform F1
between homozygous lines. The similarity between the
results obtained in Madrid and Buenos Aires, which
found no detectable environmental e€ect, reinforces the
same conclusion.
Chiavarino et al. (1998) demonstrated that, in
0B ´ 2B crosses, male B-TR depended on the 0B female
parent, irrespective of the Bs. It was therefore concluded
that the gene/genes controlling B-TR are located on the
A chromosomes. These results also indicate that the
genotype of the 0B female determines the rate at which
the egg cell is fertilized by the sperm nucleus carrying
the Bs. Therefore, a 0B female parent of the H genotype
preferentially selects the 2B sperm to fertilize the egg; in
contrast, the 0B L female does not select any sperm
nucleus, resulting in a Mendelian B-TR.
In the present work, signi®cant di€erences between
0B ´ 2B and 2B ´ 2B crosses were not found. This
indicates that male B-TR is not a€ected by the presence
of Bs in the egg-cell, which is in agreement with the
hypothesis.
Ó The Genetics Society of Great Britain, Heredity, 86, 743±748.
747
The intermediate B-TR found in the HL and LH
hybrids reported in this work further supports this
conclusion and strongly suggests that an HL or LH 0B
hybrid used as female, will produce 50% of H and 50%
of L egg-cells. The L egg cell will be fertilized by the 0B
or 2B sperm at random, whereas the H egg cell will be
preferentially fertilized by the 2B sperm. The overall
result will be an intermediate B-TR between the H and L
lines. Our hypothesis is that the gene controlling
B-TR acts in the egg cell at the haploid level during
fertilization.
Cytoplasmic maternal e€ects can be discarded. If the
high or low B-TRs were due to a maternal e€ect, HL
hybrids would show H B-TR and LH ones would show
L B-TR; however, HL and LH hybrids behaved
similarly.
The main aim of investigation into variation in B-TR
is to understand the genetic basis of B polymorphism
and, consequently, its in¯uence on genome evolution.
B chromosome evolution has been recently reviewed by
Camacho et al. (2000), who discuss the equilibrium
models of B evolution for heterotic and parasitic Bs
(Jones, 1985; Shaw & Hewitt, 1990; Bougourd et al.,
1995; Bougourd & Jones, 1997), and further develop the
nonequilibrium model based mainly on the B chromosome system of the grasshopper Eyprepocnemis plorans,
where the parasitic Bs have been neutralized by the A
genome (Camacho et al., 1997a, b; Zurita et al., 1998).
The nonequilibrium model of long-term evolution of B
chromosomes is considered to be the outcome of
selection on the host genome to eliminate B chromosomes or suppress their e€ects and on the B chromosome's ability to escape through the generation of new
variants (Camacho et al., 2000).
Our results are in agreement with Camacho's hypothesis because an H allele promoting the transmission of
the B is compatible with A and B chromosome
coevolution. Our hypothesis is that the main function
of the gene controlling B-TR that we have selected, is
not to determine B preferential fertilization rate. On the
contrary, we think that this gene, located on the As, is
involved in the normal fertilization process, but that the
Bs have an opportunistic behaviour, taking advantage
of the H function to increase their own transmission.
The L allele could be the response of the host genome to
get rid of the B e€ects. Therefore, our proposal is that
maize Bs have parasitic behaviour, using the characteristics of the normal maize fertilization process to
generate the necessary drive to invade and persist in
populations, promoting their own transmission. The
H allele, located on the A chromosomes and probably
involved in the normal process of gamete fertilization,
allows B chromosome accumulation (and hence B
chromosome attack), and another allele in the same
748
A. M. CHIAVARINO ET AL.
gene (L) is a mutation suppressing B accumulation (thus
providing A chromosome defence). The existence of the
H and L alleles as a polymorphic system of attack and
defence between A and B chromosomes is a clear
example of the coevolution of genome con¯ict as
reviewed in Frank (2000).
Acknowledgements
We thank Dr J.P.M. Camacho for his valuable comments
to the manuscript. We also thank Dr C.A. Naranjo for
his suggestions and critical comments. A.M. Chiavarino
and M. Rosato are postdoctoral grant holders of the
CONICET (Argentina). P. Rosi is a predoctoral grant
holder of the University of Buenos Aires. This work was
supported by grant 98-0678 of the DGES of Spain and
by the Agencia Nacional de PromocioÂn CientõÂ ®ca y
TecnoloÂgica, CONICET, Argentina.
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